Mating in a Material World

Some female animals don't hesitate to trade their bodies in exchange for material gain

02-01-2005
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Maggie McKee

AS ANIMAL TOTEMS GO,penguins take their place somewhere between the regal eagles and the hapless hippos. By virtue of their sleek lines, “formal wear,” and pure exotic appeal, penguins symbolize dignity and class. But their decidedly awkward waddles and round, fuzzy offspring also make them adorable and endearing.

So it might come as a surprise that, at times, penguins behave in ways that seem neither stately nor cute but rather what we humans might call sleazy. To wit, Adélie penguins regularly steal stones from other nests to fortify their own, even though they get pecked and chased in the process. More surprising yet is the recent discovery that some females resort to peddling their bodies in exchange for the precious pebbles.

And penguins are not the only creatures to exchange sex for a material benefit (aside, of course, from humans). A few other birds trade reproduction favors for food, and many insects have evolved elaborate quid pro quo sexual arrangements. In several cases, one or another of the individuals involved has even figured out a way to get something for nothing.

Animal behaviorists believe these “deals” could have evolved for several reasons: to encourage sex; to provide a kind of offspring support for the third party’s potential progeny; or to lay the groundwork for a possible future relationship. In any case, with some of the examples stretching back millions of years, prostitution seems to live up to its reputation as the oldest profession.

For Adélie penguins in Antarctica, that could be modified to the coldest profession. Every year around the end of October, about five million of these birds, which spend most of their lives in the ocean, trudge over miles of pack ice to the exposed, rocky soil of their breeding grounds. Thousands of pairs nest in one breeding site, with the pairs spaced just a couple of feet apart. Previously attached males take up residence in their old nests, shallow pits carved from the frosty Earth and carpeted with hundreds of stones the size of dates. Single males stake out and build nests of their own, in the hopes of one day starting a family.

When the females return, they choose mates from among the males on the nests, rejoining their companions from the previous year when possible.

The risk of a warm spell is what motivates the penguins’ quest for stones. Meltwater from the surrounding ice can inundate the colony and cause a breeding disaster. “Everything gets thick with mud and guano and it’s horrendous,” says Fiona Hunter, a zoologist at the University of Sheffield in England who has studied the birds in Antarctica. “The eggs can end up sitting in a pool of water, and they probably wouldn’t hatch because of the cold.” Immersion can suffocate the embryos.

A large pile of stones lifts the eggs off the ground and out of harm’s way. So males and females take turns scouring the area for unattended stones, often trying to swipe them from neighbors. The victims chase brazen robbers away by pecking them and bashing them with powerful flippers.

Given nest owners’ violent reactions to birds that try to steal their stones, Hunter was surprised and amused when she saw a female waddle off with a stone from an unattached male’s nest—while he looked on calmly. The female had just mated with him. “I thought, ‘She’s trying to do something tricky here,’” says Hunter, who had been keeping track of which penguins were paired together. She and colleague Lloyd Davis of the University of Otago in New Zealand had previously found that one out of ten females have sexual encounters with males other than their mates, but they had never seen anything like this. The researchers kept their eyes open for more cases of penguin prostitution, and they observed a total of ten over three breeding seasons.

In each case, a female penguin left her mate and made her way to a single male at his nest. She stood nearby and gazed at him. When he gave her a sidelong glance and bowed his head, she followed suit. The hopeful male then stepped off his platform of stones, allowing her to waddle on. Leaving no uncertainty about what she was there for, she lay face down on the nest, and the male mounted and mated with her. Afterward, she got up, picked up a stone with her beak, and without further ado, went back to her own nest. In half of the cases, the female returned to the same single male for a second stone, although they did not mate again. In one instance, a female made off with a total of ten stones.

And the researchers discovered another curious behavior: Often the females took stones away from the males without offering to mate in return. The females would flirt exactly as before, only they would skip the mating and take off with a stone. “It’s as if she takes the money and runs,” says Davis. Strangely, none of the males protested, though a few tried unsuccessfully to mount the females. One of the females came back for no fewer than 62 stones within an hour. “These males are not very intelligent,” jests Davis. But perhaps they’re smarter than they seem. “They want lots of offspring of the highest quality possible,” says Hunter.

Single males could be meeting those aims by trading stones for sex. “One argument is that by letting the females have the stones, every now and then the males get to copulate and get the chance to sire offspring,” says Davis. DNA tests on Adélies suggest the male who raises the chick is nearly always its father, so the encounters probably do not produce many offspring. But if the single male did succeed in fathering young, he would be getting off easy: He wouldn’t have to lift a flipper to raise them, and the stone he provided would literally give his progeny a leg up in the world.

Both Davis and Hunter caution that only a few cases of such behavior have been documented, so it’s difficult to determine the most likely motives. But to be thorough, they list several other possible interpretations of the phenomenon. The female could gain if her mate was infertile, and the “extramarital affair” ensured a successful breeding season. Or the female could be ensuring the fittest father for her chick. The sperm from each male would compete inside her to fertilize her eggs, and in theory, the “best” sperm would win.

Finally, Hunter believes the female may be checking out a potential future mate in case her current mate dies before the next breeding season, which happens to more than a quarter of the males.

The idea of females choosing their mates for genetic or other reasons pushes the bounds of classical theories about sexual selection. The old view held that males compete with each other to mate with a female, who has no choice in the matter. “Life isn’t as simple as it was thought,” says John Reynolds, a biologist at the University of East Anglia in the United Kingdom. “Females have a lot more tricks of their own than anyone had ever given them credit for.”

Other animals also prostitute themselves for something valuable to them—usually food. For female purple-throated carib hummingbirds, good meals are dependent on the three key factors in real estate: location, location, location. The males of this tropical Caribbean species are larger than females and tend to monopolize neighborhoods with the most productive flowers. Females are left to settle for skimpy plots or to scavenge for food. Perhaps it’s not surprising then that it is the females that do not pair up with long-term partners who seem to trade sex for the right to poach in male territories.

But when it comes to turning tricks, insects have no equal. And their stock-in-trade is food—the deals so common they have a name: nuptial gifts. These range from dead prey—the insect equivalent of a box of chocolates—to food bags attached to females’ bodies during mating.

“The big question from an evolutionary perspective is, why is the male investing?” asks Darryl Gwynne, an entomologist at the University of Toronto. “There are two main theories. He could be getting direct fertilization success, or he could be indirectly contributing to the welfare of his kids.” The food seems to represent an early child-support payment for the inch-long hangingflies of North America. During the mating period, females basically stop hunting, and males go after larger prey. When a male snags something, he sends out a chemical signal, or pheromone, and females make a beeline for the meal.

As the female chows down, the male begins to mate with her. But the female is rather mercenary about the whole affair: Even though they are coupled, she somehow prevents his sperm from entering her body until she has gorged herself for a full five minutes.

If, after that time, she has already devoured the insect, she will struggle to free herself from this male—he has offered her too paltry a gift. Time to move on to another john, who might provide a bigger offering. But if the gift is large enough, the male’s sperm will flow into her body for 20 minutes, when she is fully inseminated.

After 20 minutes, the male will struggle free and snatch back what’s left of his gift, either to eat it himself or to use it to lure another female. He is successful in that case: The female loses interest in sex for a few hours and lays eggs almost certainly fathered by him.

Randy Thornhill, a biologist at the University of New Mexico who literally wrote the book on the evolution of insect mating systems, says this behavior has evolved to provide females with the nourishment they need to produce eggs. And because a well-fed female runs less risk of getting tangled in spider webs while searching for food, he notes, “She gets the food she needs at lower cost than if she hunted it on her own.”

Her offspring benefit as well. The extra food makes them bigger and more resilient. “And by cutting off the copulation in five minutes,” says Thornhill, “she’s getting food but avoiding the sperm from males who might not be good hunters.”

Diversion—not nourishment—is behind the gifts of male decorated crickets. The crickets use a 200 million-year-old system in which a male attaches a bag of sperm to a female’s abdomen. It takes about 45 minutes to inseminate her, and in that time the female will reach back, remove, and eat the sperm sack itself if she isn’t distracted with another offering. So males also provide a snack—but it’s far from nutritious.

“It’s kind of a sham,” says Scott Sakaluk, an entomologist at Illinois State University. “The males are basically giving the females a big Gummy Bear. If you have the insect equivalent of a sweet tooth, males have a way to engage that without really having to spend too much on the quality of the gift.”

The Australian redbacked spider, on the other hand, could not spend more on his gift. After mating with the female, the much tinier male somersaults into her open mouth like a kamikaze pilot. His body doesn’t provide much in the way of nutrition, but it seems to keep the female busy as his sperm enters her body.

Now that’s a trick.

Maggie McKee is a science writer from Washington, D.C. This article was excerpted from a feature that originally appeared in California Wild, published by the California Academy of Sciences.